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Do gender differences influence the prevalence of sickle
cell disorder and related morbidities among school
children in rural central India?
Akre Charuhas V 1, Sukhsohale Neelam D 2*, Kubde Sanjay S 3, Agrawal Sanjay B 4,
Khamgaokar Mohan B 5, Chaudhary Sanjeev M 6, Dhoble Manjusha A 7
1
M.D.; Assistant professor, Department of Preventive and Social Medicine. Indira Gandhi Government Medical
College, Nagpur, India
2
M.D.; Assistant professor, Department of Preventive and Social Medicine. Indira Gandhi Government Medical
College, Nagpur, India
3
M.D.; Associate Professor and head, Department of Preventive and Social Medicine. Indira Gandhi
Government Medical College, Nagpur, India
4
Statistician, Department of Preventive and Social Medicine. Indira Gandhi Government Medical College,
Nagpur, India
5
M.D.; Professor and head, Department of Preventive and Social Medicine. Indira Gandhi Government
Medical College, Nagpur, India
6
M.D.; Assistant professor, Department of Preventive and Social Medicine. Indira Gandhi Government Medical
College, Nagpur, India
7
M.D.; Assistant professor, Department of Preventive and Social Medicine. Indira Gandhi Government Medical
College, Nagpur, India
* Corresponding Author: Dr. Neelam Damodar Sukhsohale
Assistant Professor, Department of Preventive and Social Medicine
Indira Gandhi Government Medical College, C.A. Road, Nagpur-18, India
Contact no: 09960390868 | Email id: bkdrneelam@gmail.com
Abstract
Background and Objectives: Sickle cell disease (SCD) is a genetic disorder of great
epidemiological, clinical and public health relevance in developing countries like India. It is
irreversible, untreatable health problem responsible for increased morbidity and mortality of
school children. With this background, the present study was undertaken to estimate the
prevalence of sickle cell disorder and associated morbidities and also to assess the gender
differences in rural school children of central India.
Methods: A cross-sectional study was carried out among 735 school going children studying
in 5th to 10th standard of Sevanand High School, Mahadula village, Koradi road district
Nagpur. Detailed information regarding socio-demographic profile was inquired. Each
student was subjected to thorough general and systemic examination. Also, haemoglobin
estimation and sickling test was performed. In addition, Haemoglobin electrophoresis was
done in students with positive sickling test.
Results: Out of total 735 students, 56.2 % were male and 43.8% were female students
belonging to different caste. 6.7% students showed sickling test positive with 30 (7.3%)
males and 19 (5.9%) females. Majority of sickle positive students were males and belonged
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to schedule caste (mahar). All sickling test positive children were found to be sickle cell trait
on haemoglobin electrophoresis. Mean haemoglobin level and mean quetelet index was found
to be significantly lower in sickle cell trait students (p<0.001). Related morbidities like
lymphadenopathy, upper respiratory tract infection, joint pain and otitis media were found in
Hb AS students with greater prevalence among male students as compared to female
students.
Conclusions: The overall prevalence of sickle cell trait was found to be 6.7% in rural school
children with higher prevalence among male students and preponderance in schedule (mahar)
caste. Also, high prevalence of anaemia and morbidities (lymphadenopathy, upper respiratory
tract infection, joint pain and otitis media) were found in sickle cell trait male students.
Key words: Sickle cell disorder, haemoglobinopathy, school children, rural.
Running title: Sickle cell disorder in rural school children
Introduction
Sickle cell disorder has remained a neglected field of research in developing countries like
India and magnitude of problem has never been appreciated in spite of the fact that the
sickled RBCs were detected in the blood of Indian patients as early as 1952. Sickle cell
disorders are a group of autosomal recessive disorders, caused by point mutation at the sixth
position in beta globin chain, valine substituting glutamic acid.1 The resultant HbS has poor
solubility in the deoxygenated state and can polymerize within the red cells. The red cell
shows a characteristic shape change because of polymer formation and becomes distorted and
rigid, the so-called sickle cell.2
Because of its prevalence and wide-spread consequences, sickle cell disease is an important
public health problem in India. Sickle cell disease is an autosomal recessive genetically
transmitted hemoglobinopathy responsible for considerable morbidity and mortality. It is one
of the most common hereditary diseases occurring worldwide, which may affect any organ or
system of human body.3 In India, sickle cell disorder is more common in central and southern
parts of the country. It is the second most common haemoglobinopathy, next to thalassemia
in India.4 School age children forms 25% of the world’s population, approximately one-fifth
of Indian population comprises of school age children. The school going age is a dynamic
period of physical growth and development, when children undergo mental, emotional and
social changes. The health status of school children varies from one place to another also
varies in urban, rural and tribal areas. The health of school children is influenced by complex
of genetic, environmental, social and economic factors.5 It was proposed that distribution of
sickle cell disorder in India has an ethnic and racial basis. Sickle cell trait in India, contrary to
view once held that it was found only in the isolated pocket, has systematic and widespread
distribution between the various tribal, rural and few other related population. Very few
studies have been conducted in school children in rural areas of Nagpur city where sickle cell
disorders are very rampant. Therefore the present study was conducted to estimate the
prevalence of sickle cell haemoglobinopathy with associated morbidities and also to assess
the gender differences in rural school children of central India.
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Methodology
A Cross sectional study was carried out among the rural school children of Sevanand High
School, Mahadula village, Koradi road district Nagpur. The school is situated 16 km away
from Indira Gandhi Government Medical College, Nagpur.
Study area
There are 6 census town in the Nagpur district (census town is that town where ¾ of the male
working population was engaged in non agriculture pursuits, if the density of population is
expected to reach the figure of 400 sq. km and minimum population for that area is 5000).
Out of which Mahadula has maximum population of schedule caste and schedule tribe as per
census (2001). There were three schools in the Mahadula village, out of which one was
selected randomly i.e. Sevanand High School, Mahadula, Nagpur.
Permission was obtained from headmaster of the school. A meeting was held before the start
of the study by calling the teachers and parents of the children. The purpose of the study in
detail was explained to them and also assured co-operation to conduct the study. There were
739 students in 5th to 10th class. There were 4 students who were absent since long period,
they were excluded from study. Hence 735 students were included in the study.
Data collection
School was visited thrice a week. During each visit near about 7 to 8 students were covered.
A rapport was established with the students and teachers. For each student detail information
regarding socio-demographic factors was obtained as per the predesigned proforma. Students
who were not present during the first visit were covered in subsequent visit. After obtaining
general information every student was subjected to thorough clinical examination and
investigation. Every student was enquired about presenting complaints as well as complaints
related to sickle cell disorder. Also, detail clinical and systemic examination was done.
Anthropometric measurements like weight and height were taken as per standard technique.6
Every student was subjected to haemoglobin estimation and sickling test. Haemoglobin
electrophoresis was done in students with positive sickling test. For this purpose, 2 ml of
venous blood was taken from every study subject by taking all aseptic precaution. This blood
sample was collected in EDTA bulb. The bulb was then labeled and packed properly and was
brought to Indira Gandhi Government Medical College, Nagpur. Haemoglobin was estimated
by Sahli’s Haemoglobinimeter method 7, 8 and sickling test was also performed.9 Sickling
positive samples were subjected to haemoglobin electrophoresis using cellulose acetate
method.9
Statistical analysis
Percentages mean and standard deviation was calculated. For statistical analysis, betweengroup comparisons were conducted using chi-square tests, Fisher’s exact test and student t
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test. Epi Info statistical package programme version 6.0. updated 2009 was used to analyse
the data. Statistical significance was assessed at a type I error rate of 0.05.
Results
Total numbers of screened students were 735, out which 413 (56.2%) were males and 322
(43.8%) were females. The demographic and other characteristics of study subjects are
shown in Table 1. Most number of students was found in the age group of 13-14 years i.e.
127 (17.3%) while least number of students found in the age group 17-18 years i.e. 33 (4.5%)
with male (17.4%) as well as female (17.1%) preponderance in the age group of 13-14 years.
As far as caste distribution of students is concerned, more students belonged to schedule caste
(mahar) i.e. 265 (36.1%), out of which 106 (32.9%) were females and 159 (38.5%) were
males; followed by other backward community, out of which 10.1% were teli, 8.7% were
Kunbi and 8.2% belonged to Mali caste. Students of other caste and sub-caste found were
scheduled tribe, nomadic tribe and vimukta jamati.
When the habits like tobacco/ghutka chewing and smoking were compared in male and
female students, it was observed that more proportion of male students (31.2%) had the habit
of tobacco/ghutka chewing and smoking (1.9%) as compared with female students (18.3%).
It was observed that out of 735 students, 49 (6.7%) showed sickling test positive out of which
30 (7.3%) boys were positive for sickling test while 19 (5.9%) girls were positive for sickling
test. However the difference between male and female students was not found to be
statistically significant (p>0.05). Moreover, the various grades of anaemia (mild, moderate
and severe) in male students were found to be statistically significant with female students
(p<0.01) as shown in Table 2.
When caste wise distribution of sickle positivity in male and female students were compared
(Table 3), it was observed that out of total 49 sickle positive students, preponderance of male
students from mahar (60%) and Teli caste (13.3%) was found as compared with female
students. Although the difference between them was not found to be statistically significant
(p>0.05). The findings are summarized in Table 3.
Haemoglobin electrophoresis of 49 sickling test positive results was found to be sickle cell
trait i.e. Hb AS. It was found that mean haemoglobin level among the sickle cell trait students
was less as compared to mean haemoglobin level among the normal students. The difference
was found to be statistically significant (p<0.001). Also, the mean Quetlet index between the
normal students (HbAA) and sickle cell trait students (HbAS) was found to be statistically
significant (p<0.001) as evident from Table 4.
Table 5 shows the various morbidities observed in HbAS male and female students. It was
seen that lymphadenopathy18 (36.8%), upper respiratory infection 9 (18.4%), joint pain 8
(16.4%), otitis media 6 (12.2%), and epistaxis 02 (4.1%) formed common morbidity in sickle
cell trait students. Although the prevalence of these morbidities were higher in male students,
the differences in morbidities between male and female students were not found to be
statistically significant (p>0.05).
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Discussion
The present study emphasized the comparative assessment of the hematological and
morbidity pattern of male and female sickle cell disease (SCD) children belonging to rural
areas. The SCD male children exhibited statistically significant (p < 0.05) lower values for all
the measurements.
As per census 2001 Mahadula and other villages have the highest population of scheduled
caste in Nagpur district. The present study reported quite high prevalence of sickle cell trait
(6.7%) with preponderance in male school students when compared with female students.
Although SCD, a genetic disorder, is prevalent in many areas of India.10 However, the
reported prevalence estimates show an enormous variation (i.e., 0–40%).11-13 Kamble M et al
11, reported incidence of sickle cell trait to be 2.17%. Sahu T et al,14 reported 16.55%
prevalence of sickle cell disorder in below fifteen years children in tribal areas of Gajapati
district of Orissa. Balgir R S et al,15 observed sickle cell disease in Bhuyan and Kharia tribes
of north-western Orissa and reported 25.5% prevalence of sickle cell disease in school
adolescents. The highest frequency of sickle cell gene in India is reported in Orissa followed
by Assam, Madhya Pradesh, Utter Pradesh, Tamilnadu and Gujarat.16 Patel A B et al,17
reported older age of presentation, absence of severe anemia, male preponderance in their
study. It indicates limited availability of health services, education and counseling available
to susceptible populations,18 which was also observed in present study.
Caste wise, the prevalence of sickle cell trait in our study was found to be highest in Mahar
i.e.36.1% followed by Teli (10.1%), Kunbi (8.7%) and Mali (8.2%). These findings are
consistent with the findings of other investigators. The study carried out by Bhobate SK et al
(1983)19 in Chandrapur district of Maharashtra in their study found sickle cell trait, 9.42%
i.e. maximum in Mahar caste and 5.06% in Teli. Kar BC (1983)20 also reported high
prevalence of sickle cell trait in Mahar (19.8%). Another study carried out by Shukla RN et al
(1958)21 among 1010 subjects in Nagpur found the prevalence of sickle cell trait about 22.2%
in Mahar and 11.3% in Teli caste. These observations support the hypothesis that the sickle
cell disorders are present in scheduled castes, tribals and few communities of OBCs and not
found in so called higher castes; though the review of literature says it is present invariably in
all castes8.
Our study also reported higher non-significant prevalence of various sickle cell related
morbidities like lymphadenopathy, upper respiratory infection, joint pain, otitis media, and
epistaxis in male SCD children. However, Bhobate SK et al in their study,19 found joint pain
to be the most prevalent morbidity.
In the present study, anemia was found to be very common morbid condition in SCD children
(Hb AS trait) as compared to normal children (Hb AA pattern) with mean hemoglobin of 7.9
± 0.635 and 10.83 ± 1.254 respectively. Kamble M. et al (2000)11 and Carol K et al (1984)22
had obtained similar findings in their study. It is believed that anemia plays a role in the
pathophysiology of SCD; however, it is not very clear whether anemia affects either specific
organ function or over-all cellular metabolism sufficiently to result in growth retardation.
Anemia can be corrected by giving multiple blood transfusions which will ultimately help to
reduce the number of cells capable of sickling to clinically insignificant levels. The steadystate hemoglobin level may have a potential impact on growth of the school children because
of its direct relationship with oxygen delivery to the tissues.23 Therefore, this study,
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specifically highlights the need of a multidimensional approach for understanding the
hematological and anthropometric variations seen among the Indian SCD rural children.
So, with the overall prevalence of sickle cell trait of 6.7% found in rural school children in
our study with higher prevalence among male students and preponderance in schedule caste
(mahar); spreading high awareness about sickle cell disease in the community becomes a
prerequisite for early detection and management of SCD particularly in school age
children. Also, since high prevalence of anaemia and related morbidities like
lymphadenopathy, upper respiratory tract infection, joint pain and otitis media found in sickle
cell trait male students in our study, efforts should be taken to reach community through
school adolescents by imparting health education to them. After completion of study, we
imparted health education to the students of each class separately regarding the sickle cell
disorder using posters and flip charts. The parents of sickle positive students were called at
school and were given health education regarding the various morbidities related to sickle
cell disorder. Also they were given the genetic counselling regarding this disorder so as to
prevent the carrier state or sickle cell disease in future generation.
Conclusions
The overall prevalence of sickle cell trait was found to be 6.7% in rural school children with
higher prevalence among male students and preponderance in schedule (mahar) caste. Also,
high prevalence of anaemia and morbidities (lymphadenopathy, upper respiratory tract
infection, joint pain and otitis media) were found in sickle cell trait male students.
In conclusion, this study highlights the need for conducting a more comprehensive study by
integrating the clinical, nutritional, and social aspects associated with SCD. Besides, a
dedicated monitoring programme for assessing hematological parameters of SCD-SS needs to
be initiated for effective management. Education for patients with SCD should focus on
specific food intake which can increase the nutritional value through various foods and can
effectively alleviate anaemia or other symptoms. Also, there is an urgent need to improve
primary health care professional training in the care of children with sickle cell disease in
areas where children with sickle cell disease are more vulnerable than adults. In this context,
it is necessary to investigate whether doctors and nurses who serve in these areas are
adequately trained and prepared to assist these children and their families. So far, the
initiatives of Indian Government have not shown great results of improving the quality of life
of SCD sufferers. Many non-governmental and voluntary organizations working for sickle
cell anemia and identification work are doing camps, where large number of people gathers,
and their blood samples are collected to carry out laboratory investigation but that`s all on
temporary basis. Unfortunately neither the diagnostic nor the treatment facilities are available
in tribal area and all this are beyond their reach. Without diagnosis and comprehensive care,
children suffer crippling medical problem leading to lack of education, employment
opportunities and integration into the society. Therefore the limited availability of medical
and health care in rural areas, as well as other support systems calls for an increase in
community based healthcare services.
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List of abbreviations:
SCD: Sickle cell disease
OBC: other backward community
Hb AA: Haemoglobin AA (normal adult pattern)
Hb AS: Haemoglobin AS (sickle cell) trait
IRB permissions
The project has been approved by Clinical ethics Committee, Indira Gandhi Government
Medical College, Nagpur
Approval date: 27-04-01
IRB permission number: 10/17/3/01
Grant Registration Number: This is a non-funded study
Competing interests: Nil
Acknowledgements: None
References
1. Deshmukh P. et al. Prevalence of Sickle Cell Disorders in Rural Wardha. Indian Journal
of Community Medicine 2006; 31(1):26-27.
2. Doshi Neena, Chaudhari Sanjay, Shah Nigam, Joshi Trupti1, Shah Menka1, Uday Singh.
Prevalence of sickle cell disorder in rural Pipalwada, Gujarat. National Journal of
Community Medicine 2011;2(2):284-288.
3. Kamble M, Chatruvedi P. Epidemiology of sickle cell disease in a rural hospital of
central India. Indian Pediatrics 2000;37:391-396.
4. Agarwal MB, Mehta BC. Sickle syndrome - A study of 44 cases from Bombay. Indian
Paediatrics 1980;17:793.
5. World Health Organisation: Health needs of adolescent – report of WHO expert
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6. Jelliffe DB. The assessment of nutritional status of community, WHO, Geneva
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7. Mahapatra ABS. Essential of Medical Physiology. 1st edition 1998;31-2.
8. Chatterjee CC. Human Physiology. 1998;157-8.
9.
John Bernard Henry. Clinical Diagnosis and Management by Laboratory Test.19th ed.,
W.B. Sunders Company,1996.
10. Balgir RS. Phenotypic diversity of sickle cell disorders with special emphasis on public
health genetics in India. Curr Sci 2010;98:1096–102.
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11. Kamble M, Chaturvedi P. Epidemiology of sickle cell disease in a rural hospital of
central India. Indian Pediatrics. 2000;37:391–6.
12. Deshmukh P, Garg BS, Garg N, Prajapati NC, Bharambe MS. Prevalence of sickle cell
disorders in rural Wardha. Indian Journal of Community Medicine 2006;31:26–7.
13. Serjeant GR. The case
Genet. 2006;12:148–51.
for
dedicated
sickle
cell
centres. Indian
J
Hum
14. Sahu T, Sahani NC, Das S, Sahu SK. Sickle cell anemia in tribal children of Gajapati
district in south Orissa. Indian Journal of Community Medicine. 2003;28:180-183.
15. Balgir RS. The spectrum of hemoglobin variants in two scheduled tribes of Sundargarh
district in north-western Orissa, India. Annals of Human Biology. 2005; 32:560-573.
16. Balgir RS. Genetic epidemiology of the three predominant abnormal hemoglobins in
India. JAPI. 1996; 44:25-8.
17. Patel AB, Athavale AM. Sickle cell disease in central India. Indian J Pediatr. 2004;71:
789-793.
18. Patra PK, Tripathi S, Khodiar P, Dalla AR, Manikpuri PK, Sinha A. A study of carrier
status of sickle cell disease among inmates of central jail Raipur (Chhattisgarh). J Comm
Med. 2008;4:11-12.
19. Bhobate SK, Kabinwar N, Sonule SS. Incidence of sickle cell disease in Chandrapur
area. Indian J Med Science. 1983;37(11):201-3.
20. Kar BC. Sickle cell anaemia in tribes of Orissa. JAPI 1983;31(5):321-5.
21. Shukla RN, Solanki BR, Parande AS. Sickle cell disease in India. Indian J Med Sciences.
1958;892.
22. Phebus CK, Gloninger MF, Maciak BJ. Growth pattern by age and sex in children with
sickle cell disease. J Pediatric. 1984;105(1):28-32.
23. Animasahun BA, Temiye EO, Ogunkunle OO, Izuora AN, Njokanma OF. The influence
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Table 1: Demographic and other characteristics of study subjects
Characteristic
Age (years)
10-11
11-12
12-13
13-14
14-15
15-16
16-17
17-18
Caste
Schedule caste: Mahar
Other backward community:
Teli
Kunbi
Mali
Sonar
other OBC
Schedule tribe:
Gond
Gowari
Lohar
Thakur
Nomadic tribe:
Dhivar
Kirat
Ahir
Beldar
Vimukta jamati:
Rajput
Lodhi
Other caste
Habits: 1.Tobacco/Ghutka chewing
2. Smoking
3. Multiple habits
4. No habits
Figures in parentheses indicate percentage.
Total
(N = 735)
Male students
413 (56.2%)
Female students
322 (43.8%)
61 (14.8)
60 (14.5)
58 (14.0)
72 (17.4)
52 (12.6)
46 (11.1)
44 (10.7)
20 (4.8)
50 (15.5)
53 (16.5)
49 (15.2)
55 (17.1)
48 (14.9)
32 (9.9)
22 (6.8)
13 (4.0)
111 (15.1)
113 (15.4)
107 (14.6)
127 (17.3)
100 (13.6)
78 (10.6)
66 (9.0)
33 (4.5)
159 (38.5)
38 (9.2)
106 (32.9)
36 (11.2)
265 (36.1)
74 (10.1)
36 (8.7)
36 (8.7)
10 (2.4)
12 (2.9)
24(5.8)
14 (3.4)
16 (3.9)
09 (2.2)
05 (1.2)
12 (2.9)
06 (1.5)
04 (1.0)
06 (1.5)
03 (0.7)
23 (5.6)
129 (31.2)
8 (2.0)
14 (3.4)
262 (63.4)
28 (8.7)
24 (7.5)
08 (2.5)
09 (2.8)
26 (8.1)
14 (4.3)
10 (3.1)
02 (0.6)
03 (0.9)
07 (2.2)
06 (1.9)
04 (1.2)
09 (2.8)
04 (1.2)
26 (8.1)
59 (18.3)
0
0
263 (81.7)
64 (8.7)
60 (8.2)
18 (2.5)
21 (2.9)
50 (6.8)
28 (3.9)
26 (3.5)
11 (1.5)
08 (1.1)
19 (2.6)
12 (1.6)
08 (1.1)
15 (2.1)
07 (1.0)
49 (6.7)
188 (25.6)
8 (1.1)
14 (1.9)
525 (71.4)
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Table 2: Distribution of subjects according to sickling positivity and grades of anaemia
Male
students
(N = 413)
Female
students
(N = 322)
Total
(N = 735)
30 (7.3)
19 (5.9)
49 (6.7)
Normal
96 (23.2)
45 (14.0)
141 (19.2)
Mild
199 (48.2)
186 (57.8)
385 (52.4)
Characteristic
Sickling test
positive
χ2
df 1
p value
0.54
0.46
Grades of anaemia:
Normal Vs other
grades
10.03
Moderate
Severe
114 (27.6)
88 (27.3)
202 (27.7)
4 (1.0)
03 (0.9)
7 (0.9)
0.001
Figures in parentheses indicate percentage.
Table 3: Caste – wise distribution of sickle positive students
Caste
Male
students
(N = 30)
Female
Students
(N = 19)
Total sickle
positive students
(N = 49)
Mahar
18 (60)
11(57.9)
29 (59.2)
0.42
0.51
Teli
4 (13.3)
2 (10.5)
06 (12.2)
0.26
0.60
Gond
2 (6.7)
2 (10.5)
04 (8.2)
-
Mali
1(3.3)
2 (10.5)
03 (6.1)
-
Kirat
1(3.3)
1(5.3)
02 (4.1)
-
Thakur
0
2 (10.5)
02 (4.1)
-
Sheikh
1(3.3)
0
01 (2.0)
-
Kunbi
1(3.3)
0
01 (2.0)
-
Gowari
0
1(5.3)
01 (2.0)
-
χ2
df 1
p value
Figures in parentheses indicate percentage.
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358
Table 4: Mean Haemoglobin level and Mean Quetelet index in Hb AA and Hb AS students
Mean
haemoglobin
level ± S.D.
Z test
Mean
Quetelet index
± S.D.
Z test
Electrophoretic
pattern
No. of
students
(N = 735)
Hb AA
686 (93.3) 10.83 ±1.254
28.08
0.148 ± 0.0089
6.23
Hb AS
49 (6.7)
<0.001
0.141 ± 0.0075
<0.001
7.95 ± 0.635
P value
P value
Figures in parentheses indicate percentage.
Table 5: Distribution of subjects according to morbidities in HbAS students
Male
Female
Total
χ2
Morbid condition
(N = 29)
(N = 14)
(N = 43)
df 1
p value
Lymphadenopathy
12 (40)
6 (31.6)
18 (36.8) 0.008
0.92
Upper respiratory tract
infection
6 (20)
3 (15.8)
09 (18.4) 0.003
0.95
Joint pain
5 (16.7)
3 (15.8)
08 (16.4) 0.10
0.74
Otitis media
5 (16.7)
1 (5.3)
06 (12.2) 0.80
0.37
Epistaxis
1(3.3)
1 (5.3)
02 (4.1)
0.58
0.29
Figures in parentheses indicate percentage.
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